Active surveillance for antibodies confirms circulation of lyssaviruses in Palearctic bats

. 2020 Dec 10 ; 16 (1) : 482. [epub] 20201210

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33302915

Grantová podpora
17-20286S Grantová Agentura České Republiky
Grant No. KП-06-H31/14 Ministry of Education, Youth and Science

Odkazy

PubMed 33302915
PubMed Central PMC7731468
DOI 10.1186/s12917-020-02702-y
PII: 10.1186/s12917-020-02702-y
Knihovny.cz E-zdroje

BACKGROUND: Palearctic bats host a diversity of lyssaviruses, though not the classical rabies virus (RABV). As surveillance for bat rabies over the Palearctic area covering Central and Eastern Europe and Siberian regions of Russia has been irregular, we lack data on geographic and seasonal patterns of the infection. RESULTS: To address this, we undertook serological testing, using non-lethally sampled blood, on 1027 bats of 25 species in Bulgaria, the Czech Republic, Poland, Russia and Slovenia between 2014 and 2018. The indirect enzyme-linked immunosorbent assay (ELISA) detected rabies virus anti-glycoprotein antibodies in 33 bats, giving an overall seroprevalence of 3.2%. Bat species exceeding the seroconversion threshold included Myotis blythii, Myotis gracilis, Myotis petax, Myotis myotis, Murina hilgendorfi, Rhinolophus ferrumequinum and Vespertilio murinus. While Myotis species (84.8%) and adult females (48.5%) dominated in seropositive bats, juveniles of both sexes showed no difference in seroprevalence. Higher numbers tested positive when sampled during the active season (10.5%), as compared with the hibernation period (0.9%). Bat rabies seroprevalence was significantly higher in natural habitats (4.0%) compared with synanthropic roosts (1.2%). Importantly, in 2018, we recorded 73.1% seroprevalence in a cave containing a M. blythii maternity colony in the Altai Krai of Russia. CONCLUSIONS: Identification of such "hotspots" of non-RABV lyssavirus circulation not only provides important information for public health protection, it can also guide research activities aimed at more in-depth bat rabies studies.

CEITEC Central European Institute of Technology University of Veterinary and Pharmaceutical Sciences Brno Brno Czech Republic

Centre for Cartography of Fauna and Flora Antoličičeva 1 SI 2204 Miklavž na Dravskem polju Slovenia

Department of Biochemistry Ural State Medical University Repina 3 620014 Ekaterinburg Russia

Department of Botany and Zoology Masaryk University Kotlářská 267 2 611 37 Brno Czech Republic

Department of Ecology and Diseases of Game Fish and Bees University of Veterinary and Pharmaceutical Sciences Brno Palackého tř 1946 1 612 42 Brno Czech Republic

Department of Ecosystem Research Environment Risk Assessment and Conservation Biology Institute of Biodiversity and Ecosystem Research Tsar Osvoboditel 1 1000 Sofia Bulgaria

Department of Infectious Diseases and Microbiology University of Veterinary and Pharmaceutical Sciences Brno Palackého tř 1946 1 612 42 Brno Czech Republic

Institute of Biology and Soil Science Far East Branch of the Russian Academy of Sciences Pr t 100 letiya Vladivostoka 159 690022 Vladivostok Russia

Institute of Biology Department of Vertebrate Ecology and Palaeontology Wrocław University of Environmental and Life Sciences Wrocław Poland

Institute of Vertebrate Biology Czech Academy of Sciences Květná 8 603 65 Brno Czech Republic

Irkutsk State Medical University Krasnogo Vosstania street 1 664003 Irkutsk Russian Federation

Land Use and Biodiversity International Complex Research Laboratory for Study of Climate Change Tyumen State University Volodarckogo 6 625003 Tyumen Russia

Western Baikal protected areas Federal State Budgetary Institution Zapovednoe Pribaikalye Baikalskaya st 291B 664050 Irkutsk Russia

Zobrazit více v PubMed

Malerczyk C, Freuling C, Gniel D, Giesen A, Selhorst T, et al. Cross-neutralization of antibodies induced by vaccination with purified chick embryo cell vaccine (PCECV) against different Lyssavirus species. Hum Vaccin Immunother. 2014;10:2799–804. doi: 10.4161/21645515.2014.972741. PubMed DOI PMC

Hampson K, Coudeville L, Lembo T, Sambo M, Kieffer A, Attlan M, et al. Estimating the global burden of endemic canine rabies. PLoS Negl Trop Dis. 2015;9:e0003709. doi: 10.1371/journal.pntd.0003709. PubMed DOI PMC

Slate D, Rupprecht CC, Rooney JA, Donovan D, Lein DH, Chipman RH. Status of oral rabies vaccination in wild carnivores in the United States. Virus Res. 2005;111:68–76. doi: 10.1016/j.virusres.2005.03.012. PubMed DOI

Slate D, Algeo TP, Nelson KM, Chipman RB, Donovan D, et al. Oral Rabies Vaccination in North America: Opportunities, Complexities, and Challenges. PLOS Negl Trop Dis. 2009;3(12):e549. doi: 10.1371/journal.pntd.0000549. PubMed DOI PMC

Wasniewski M, Almeid I, Baur A, Bedekovic T, Boncea D, Chaves LB, et al. First international collaborative study to evaluate rabies antibody detection method for use in monitoring the effectiveness of oral vaccination programmes in fox and raccoon dog in Europe. J Virol Methods. 2016;238:77–85. doi: 10.1016/j.jviromet.2016.10.006. PubMed DOI

Robardet E, Bosnjak D, Englund L, Demetriou P, Martín PR, Cliquet F. Zero Endemic Cases of Wildlife Rabies (Classical Rabies Virus, RABV) in the European Union by 2020: An Achievable Goal. Trop Med Infect Dis. 2019;4:124. doi: 10.3390/tropicalmed4040124. PubMed DOI PMC

Botvinkin AD, Poleschuk EM, Kuzmin IV, Borisova TI, Gazaryan SV, Yager P, et al. Novel lyssaviruses isolated from bats in Russia. Emerg Infect Dis. 2003;9:1623–5. doi: 10.3201/eid0912.030374. PubMed DOI PMC

Fooks AR, Brookes S, Johnson N, McElhinney LM, Hutson AM. European bat lyssaviruses: an emerging zoonosis Epidemiol Infect. 2003;131:1029–1039. PubMed PMC

Kuzmin IV, Orciari LA, Arai YT, Smith JS, Hanlon CA, Kameoka Y, et al. Bat lyssaviruses (Aravan and Khujand) from Central Asia: phylogenetic relationships according to N, P and G gene sequences. Virus Res. 2003;97:65–79. doi: 10.1016/S0168-1702(03)00217-X. PubMed DOI

Vos A, Kaipf I, Denzinger A, Fooks AR, Johnson N, Müller T. European bat lyssaviruses - an ecological enigma. Acta Chiropterol. 2007;9:283–96. doi: 10.3161/1733-5329(2007)9[283:EBLAEE]2.0.CO;2. DOI

Johnson N, Selden D, Parsons G, Healy D, Brookes SM, McElhinney LM, Hutson AM, Fooks AR. Isolation of a European Bat Lyssavirus type 2 from a Daubentons bat in the United. Kingdom Vet Rec. 2003;152:383–38. doi: 10.1136/vr.152.13.383. PubMed DOI

Johnson N, Vos A, Freuling C, Tordo N, Fooks AR, Müller T. Human rabies due to lyssavirus infection of bat origin. Vet Microbiol. 2010;142:151–9. doi: 10.1016/j.vetmic.2010.02.001. PubMed DOI

Ceballos NA, Morón SV, Berciano JM, Nicolás O, López CA, Juste J, et al. Novel lyssavirus in bat, Spain. Emerg Infect Dis. 2013;19:793–5. doi: 10.3201/eid1905.121071. PubMed DOI PMC

Freuling CM, Beer M, Conraths FJ, Finke S, Hoffmann B, Keller B, et al. Novel lyssavirus in Natterer’s bat, Germany. Emerg Infect Dis. 2011;17:1519–22. PubMed PMC

Schatz J, Fooks AR, Mcelhinney L, Horton D, Echevarria J, Vázquez-Moron S, et al. Bat Rabies Surveillance in Europe. Zoonoses Public HLTH. 2013;60:22–34. doi: 10.1111/zph.12002. PubMed DOI

Banyard AC, Evans JS, Luo TR, Fooks AR. Lyssaviruses and bats: emergence and zoonotic threat. Viruses. 2014;6(8):2974–90. doi: 10.3390/v6082974. PubMed DOI PMC

Blackwood JC, Streicker DG, Altizer S, Rohani P. Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats. PNAS. 2013;110:20837. doi: 10.1073/pnas.1308817110. PubMed DOI PMC

Colombi D, Serra-Cobo J, Métras R, Apolloni A, Poletto Ch, et al. Mechanisms for lyssavirus persistence in non-synanthropic bats in Europe: insights from a modeling study. Sci Rep. 2019;9:537. doi: 10.1038/s41598-018-36485-y. PubMed DOI PMC

Van Der Poel WHM, Van Der Heide R, Verstraten E, Takumi K, Lina PHC, Kramps JA. European bat lyssaviruses, the Netherlands. Emerg Infect Dis. 2005;11:1854–9. doi: 10.3201/eid1112.041200. PubMed DOI PMC

Hajkova P, Pikula J. Veterinary treatment of evening bats (Vespertilionidae) in the Czech Republic. Vet Rec. 2007;161:139–40. doi: 10.1136/vr.161.4.139. PubMed DOI

Amengual B, Bourhy H, López-Roig M, Serra-Cobo J. Temporal dynamics of European bat lyssavirus type 1 and survival of Myotis myotis bats in natural colonies. PLoS ONE. 2007;2:e566. doi: 10.1371/journal.pone.0000566. PubMed DOI PMC

Picard-Meyer E, Dubourg-Savage MJ, Arthur L, Barataud M, Bécu D, Bracco S, et al. Active surveillance of bat rabies in France: A 5-year study (2004–2009) Vet Microbiol. 2011;51:390–5. doi: 10.1016/j.vetmic.2011.03.034. PubMed DOI

Nokireki T, Huovilainen A, Lilley T, Kyheröinen EM, Ek-Kommonen C, Sihvonen L, et al. Bat rabies surveillance in Finland. BMC Vet Res. 2013;9:174. doi: 10.1186/1746-6148-9-174. PubMed DOI PMC

Robardet E, Borel C, Moinet M, Jouan D, Wasniewski M, Barrat J, et al. Longitudinal survey of two serotine bat (Eptesicus serotinus) maternity colonies exposed to EBLV-1 (European Bat Lyssavirus type 1): Assessment of survival and serological status variations using capture-recapture models. PLoS Negl Trop Dis. 2017;11:e0006048. doi: 10.1371/journal.pntd.0006048. PubMed DOI PMC

Leopardi S, Priori P, Zecchin B, Poglayen G, Trevisiol K, Lelli D, et al. Active and passive surveillance for bat lyssaviruses in Italy revealed serological evidence for their circulation in three bat species. Epidemiol Infect. 2018;1–6. PubMed PMC

Šimić I, Lojkić I, Krešić N, Cliquet F, Picard-Meyer E, Wasniewski M, et al. Molecular and serological survey of lyssaviruses in Croatian bat populations. BMC Vet Res. 2018;14(1):274. doi: 10.1186/s12917-018-1592-z. PubMed DOI PMC

Pikula J, Bandouchova H, Novotny L, Meteyer CU, Zukal J, Irwin N, et al. Histopathology confirms white-nose syndrome in bats in Europe. J Wildl Dis. 2012;48:207–11. doi: 10.7589/0090-3558-48.1.207. PubMed DOI

Zukal J, Bandouchova H, Bartonička T, Berkova H, Brack V, Brichta J, et al. White-nose syndrome fungus: A generalist pathogen of hibernating bats. PLoS ONE. 2014;9:e97224. doi: 10.1371/journal.pone.0097224. PubMed DOI PMC

Bandouchova H, Bartonicka T, Berkova H, Brichta J, Cerny J, Kovacova V, et al. Pseudogymnoascus destructans: Evidence of virulent skin invasion for bats under natural conditions, Europe. Transbound Emerg Dis. 2015;62:1–5. doi: 10.1111/tbed.12282. PubMed DOI

Flieger M, Bandouchova H, Cerny J, Chudickova M, Kolarik M, Kovacova V, et al. Vitamin B2 as a virulence factor in Pseudogymnoascus destructans skin infection. Sci Rep. 2016;6:33200. doi: 10.1038/srep33200. PubMed DOI PMC

Zukal J, Bandouchova H, Brichta J, Cmokova A, Jaroň KS, Kolařík M, et al. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci Rep. 2016;6:19829. doi: 10.1038/srep19829. PubMed DOI PMC

Pikula J, Bandouchova H, Kovacova V, Linhart P, Piacek V, Zukal J. Reproduction of rescued Vespertilionid bats (Nyctalus noctula) in captivity: Veterinary and physiologic aspects. Veterinary Clinics of North America. Exot Anim Pract. 2017;20:665–77. doi: 10.1016/j.cvex.2016.11.013. PubMed DOI

Bandouchova H, Bartonička T, Berkova H, Brichta J, Kokurewicz T, Kovacova V, et al. Alterations in the health of hibernating bats under pathogen pressure. Sci Rep. 2018;8:6067. doi: 10.1038/s41598-018-24461-5. PubMed DOI PMC

Kovacova V, Zukal J, Bandouchova H, Botvinkin AD, Harazim M, Martínková N, et al. White-nose syndrome detected in bats over an extensive area of Russia. BMC Vet Res. 2018;14:192. doi: 10.1186/s12917-018-1521-1. PubMed DOI PMC

Martínková N, Pikula J, Zukal J, Kovacova V, Bandouchova H, Bartonička T, et al. Hibernation temperature-dependent Pseudogymnoascus destructans infection intensity in Palearctic bats. Virulence. 2018;9(1):1734–50. doi: 10.1080/21505594.2018.1548685. PubMed DOI PMC

Zahradníková A, Kovacova V, Martínková N, Orlova MV, Orlov OL, et al. Historic and geographic surveillance of Pseudogymnoascus destructans possible from collections of bat parasites. Transbound Emerg Dis. 2018;65:303–8. doi: 10.1111/tbed.12773. PubMed DOI

Davy CM, Donaldson ME, Bandouchova H, Breit AM, Dorville N, Dzal YA, et al. Transcriptional host-pathogen responses of Pseudogymnoascus destructans and three species of bats with white-nose syndrome. Virulence. 2020;11(1):781–94. doi: 10.1080/21505594.2020.1768018. PubMed DOI PMC

Schatz J, Teifke JP, Mettenleiter TC, Aue A, Stiefel D, Müller T, et al. Lyssavirus distribution in naturally infected bats from Germany. Vet Microbiol. 2014;169:33–41. doi: 10.1016/j.vetmic.2013.12.004. PubMed DOI

Serra-Cobo J, Amengual B, Abellán C, Bourhy H. European bat lyssavirus infection in Spanish bat populations. Emerg Infect Dis. 2002;8:413–20. doi: 10.3201/eid0804.010263. PubMed DOI PMC

Baker M, Schountz LT, Wang LF. Antiviral immune responses of bats: A review. Zoonoses Public HLTH. 2013;60:104–16. doi: 10.1111/j.1863-2378.2012.01528.x. PubMed DOI PMC

Pikula J, Heger T, Bandouchova H, Kovacova V, Nemcova M, et al. Phagocyte activity reflects mammalian homeo- and hetero-thermic physiological states. BMC Vet Res. 2020;16(1):1–13. doi: 10.1186/s12917-020-02450-z. PubMed DOI PMC

Heger T, Zukal J, Seidlová V, Němcová M, Nečas D, et al. Measurement of phagocyte activity in heterotherms. Acta Veterinaria Brno. 2020;89(1):79–87. doi: 10.2754/avb202089010079. DOI

He X, Korytář T, Zhu Y, Pikula J, Bandouchova H, Zukal J, et al. Establishment of Myotis myotis cell lines - model for investigation of host-pathogen interaction in a natural host for emerging viruses. PLoS ONE. 2014;9:e109795. doi: 10.1371/journal.pone.0109795. PubMed DOI PMC

Brookes SM, Parsons G, Johnson N, McElhinney LM, Fooks AR. Rabies human diploid cell vaccine elicits cross-neutralising and cross-protecting immune responses against European and Australian bat lyssavirusses. Vaccine. 2005;23(32):4101–9. doi: 10.1016/j.vaccine.2005.03.037. PubMed DOI

Brookes SM, Healy DM, Fooks AR. Ability of rabies vaccine strains to elicit crossneutralising antibodies. Dev Biol (Basel) 2006;125:185–93. PubMed

Malerczyk C, Selhorst T, Tordo N, Moore S, Müller T. Antibodies induced by vaccination with purified chick embryo cell culture vaccine (PCECV) cross-neutralize non-classical bat lyssavirus strains. Vaccine. 2009;27:5320–5. doi: 10.1016/j.vaccine.2009.06.095. PubMed DOI

Reynes J-M, Molia S, Audry L, Hout S, Ngin S, Walston J, et al. Serologic evidence of lyssavirus infection in bats, Cambodia. Emerg Infect Dis. 2004;10:2231–4. doi: 10.3201/eid1012.040459. PubMed DOI PMC

Nguyen AT, Nguyen TT, Noguchi A, et al. Bat lyssaviruses, northern Vietnam. Emerg Infect Dis. 2014;20(1):161–3. doi: 10.3201/eid2001.130813. PubMed DOI PMC

Wasniewski M, Labbe A, Tribout L, Rieder J, Labadie A, Schereffer JL, et al. Evaluation of a rabies ELISA as an alternative method to seroneutralisation tests in the context of international trade of domestic carnivores. J Virol Methods. 2014;195:211–20. doi: 10.1016/j.jviromet.2013.10.021. PubMed DOI

Smits GP, van Gageldonk PG, Schouls LM, van der Klis FR, Berbers GAM. Development of a Bead-Based Multiplex Immunoassay for Simultaneous Quantitative Detection of IgG Serum Antibodies against Measles, Mumps, Rubella, and Varicella-Zoster Virus. Clin Vaccine Immunol. 2012;19:396. doi: 10.1128/CVI.05537-11. PubMed DOI PMC

Ruedi M, Stadelmann B, Gager Y, Douzery EJP, Francis CM, Lin LK, Guillen-Servent A, Cibois A. Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera) Mol Phylogenet Evol. 2013;69:437–49. doi: 10.1016/j.ympev.2013.08.011. PubMed DOI

Datzmann T, Dolch D, Batsaikhan N, Kiefer A, Helbig-Bonitz M, et al. Cryptic diversity in Mongolian vespertilionid bats (Vespertilionidae, Chiroptera, Mammalia). Results of the Mongolian–German biological expeditions since 1962, No. 299. Acta Chiropterol. 2012;14:243–64. doi: 10.3161/150811012X661594. DOI

Matveev VA, Kruskop SV, Kramerov DA. Revalidation of Myotis petax Hollister, 1912 and its new status in connection with M. daubentonii (Kuhl, 1817) (Vespertilionidae, Chiroptera) Acta Chiropterol. 2005;7:23–37. doi: 10.3161/1733-5329(2005)7[23:ROMPHA]2.0.CO;2. DOI

Streicker DG, Winternitz JC, Satterfield DA, Condori-Condori RE, Broos A, Tello C, et al. Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies. PNAS. 2016;113(39):10926. doi: 10.1073/pnas.1606587113. PubMed DOI PMC

Bouma HR, Carey HV, Kroese FGM. Hibernation: the immune system at rest? J Leukoc Biol. 2010;88:619–24. doi: 10.1189/jlb.0310174. PubMed DOI

Serra-Cobo J, López-Roig M, Seguí M, Sánchez LP, Nadal J, et al. Ecological Factors Associated with European Bat Lyssavirus Seroprevalence in Spanish Bats. PLoS ONE. 2013;8:e64467. doi: 10.1371/journal.pone.0064467. PubMed DOI PMC

Brunet-Rossinni A, Kwilkinson GS. Methods for age estimation and the study of senescence in bats.2009; In: Ecological and Behavioral Methods for the Study of Bats (eds Kunz, T. H. and Parsons, S.) 315–325 (The Johns Hopkins University Press, 2009).

Pikula J, Amelon SK, Bandouchova H, Bartonicka T, Berkova H, Brichta J, et al. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS ONE. 2017;12:e0180435. doi: 10.1371/journal.pone.0180435. PubMed DOI PMC

Servat A, Feyssaguet M, Blanchard I, Morize JL, Schereffer JL, Boue F, et al. A quantitative indirect ELISA to monitor the effectiveness of rabies vaccination in domestic and wild carnivores. J Immunol Methods. 2007;318:1–10. doi: 10.1016/j.jim.2006.07.026. PubMed DOI

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